0595
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http://www.vanderveer.org.nz/research/publications/papers/0595.pdfTRANSCRIPT
ORIGINAL PAPER
Pharyngeal Pressures During Swallowing Within and AcrossThree Sessions: Within-Subject Variance and Order Effects
Phoebe R. Macrae • Daniel J. Myall •
Richard D. Jones • Maggie-Lee Huckabee
Received: 6 May 2010 / Accepted: 21 December 2010
� Springer Science+Business Media, LLC 2011
Abstract No studies have investigated within-subject
variation in measures of pharyngeal pressures during
swallowing across sessions. This study aimed to document
the variation in pharyngeal pressures both within and
across three sessions. Twenty healthy participants were
recruited for three sessions. For each session, peak or nadir
pressures were recorded from the upper pharynx (sensor 1),
mid-pharynx (sensor 2), and upper esophageal sphincter
(sensor 3) during saliva and 10-ml water bolus swallows.
Variance was larger across sessions than within sessions
for sensors 1 and 2 but comparable for sensor 3. For all
sensors there was a high correlation between the variance
across sessions and within session (r = 0.92, p \ 0.0001).
There were no significant order effects of session or of trial
at any sensor with estimated order effects less than 2% and
the estimated maximum possible change no larger than 5%
for trial and no larger than 12% for session. These data
offer direction for longitudinal treatment studies in which
pharyngeal pressures are an outcome measurement by (1)
providing a basis for power calculations, (2) estimating the
likely values of any confounding order effects, and (3)
providing suggestions for more reliable data analysis.
Keywords Swallowing � Pharyngeal � Upper esophageal
sphincter � Pressures � Variance � Deglutition � Deglutition
disorders
Pharyngeal manometry is frequently used to document the
changes associated with various swallowing techniques in
both healthy [1–5] and dysphagic participants [6, 7]. These
studies have evaluated immediate maneuver effects by
comparing the pressure generated for dry swallows with
that generated within the same session for maneuver
swallows such as the effortful swallow [1–7], Mendelsohn
maneuver [7], supraglottic swallow [1, 6, 7], tongue-hold
maneuver [7, 8], and chin-tuck maneuver [7, 8]. Changes in
pressure have also been evaluated for differing bolus sizes
[4, 9]. For these studies, it is assumed that within-session
manometric measures are reliable and repeatable provided
various maneuver swallows are counterbalanced and
catheter placement remains stable throughout the session.
The reliability of pharyngeal pressure measures obtained
over separate sessions is not known. One study has
reported acquisition of pharyngeal pressures over two
sessions but the researchers normalized the data to account
for potential intersession variability [3]. Intersession vari-
ability could potentially result from discrepancies in cath-
eter position in the pharynx from placement to placement.
A study designed to assess the position of a pharyngeal
manometric catheter in the pharynx, when placed in one
Presented at the 18th Annual Meeting of the Dysphagia Research
Society, San Diego, CA, March 2010.
P. R. Macrae � R. D. Jones � M.-L. Huckabee
Department of Communication Disorders,
University of Canterbury, Christchurch, New Zealand
P. R. Macrae (&) � D. J. Myall � R. D. Jones � M.-L. Huckabee
Van der Veer Institute for Parkinson’s and Brain Research,
66 Stewart Street, Christchurch 8011, New Zealand
e-mail: [email protected]
R. D. Jones
Department of Medicine, University of Otago, Christchurch,
New Zealand
R. D. Jones
Department of Medical Physics and Bioengineering,
Canterbury District Health Board, Christchurch, New Zealand
123
Dysphagia
DOI 10.1007/s00455-010-9324-y
naris and then the other, found the catheter to sit at midline
for both placements in only one of ten participants [10].
Furthermore, this study found that in some cases lateral
position of the catheter is dependent on the naris in which
the catheter is inserted.
Treatment studies that utilize manometry as an outcome
measure to document changes in pharyngeal pressure
require assurance of measurement stability to attribute any
changes to treatment. No studies have investigated the
variation that results from simply removing and replacing a
manometric catheter in a participant’s pharynx.
The aim of this study was to document the variation in
pharyngeal manometric measures across swallows within
the same session and across three sessions. These data
provide information on the variance introduced into pha-
ryngeal pressure measures as a function of catheter place-
ment, thus allowing for elucidation of treatment effects
from methodological error in rehabilitation studies using
normal participants, and a reference by which to evaluate
the variance in dysphagic participants.
Methods
Participants
Twenty healthy participants (gender equally represented,
age range 18–35 years) were recruited for this study. They
reported no history of dysphagia or neurological impair-
ment. Ethical approval was obtained from the local insti-
tutional review board. Informed consent was obtained prior
to commencement of data collection.
Instrumentation
A 100-cm-long round catheter, 2.1 mm in diameter (Model
CTS3 ? EMG, Gaeltec, Hackensack, NJ), was used for
manometric data collection. The catheter houses three
solid-state, unidirectional, posteriorly oriented sensors
(2 9 5 mm), with 20 mm between sensors 1 and 2 and
30 mm between sensors 2 and 3 (as recommended in [11]).
Data were collected using the Kay Elemetrics Digital
Swallowing Workstation (Kay Elemetrics, Lincoln Park,
NJ). Digitized 12-bit samples were obtained with a sam-
pling frequency of 500 Hz and displayed in a -100 to
500-mmHg display window. The system software gener-
ates pressure waveforms as a function of time. The catheter
was calibrated at 250 mmHg at room temperature. All
measurements were displayed on a computer monitor
during data collection and digitally recorded for offline
analysis.
Procedures
Participants were seated upright in a dental chair. Each
participant completed three sessions, with a wide range of
intersession intervals (from 30 min to 7 days) to minimize
possible bias introduced by a single fixed interval. For
session 1, the lubricated intraluminal catheter was inserted
into one naris. Once the tip of the catheter reached the
upper pharynx, identified by resistance at the posterior
pharyngeal wall, the participant ingested water rapidly
through a straw until the catheter was pulled down
approximately 35 cm into the proximal esophagus. The
catheter was then pulled back out at increments of 10 mm,
until high pressure in sensor 1, the uppermost sensor,
suggested placement in the high-pressure zone of the
cricopharyngeus muscle [12]. Pull-through was then done
in 5-mm increments, requiring the participant to sit sta-
tionary and dry swallow once after a period of approxi-
mately 30 s at each increment. Pull-through was continued
until correct catheter placement was confirmed through
visualization of the typical ‘‘M’’ wave displayed at sensor 3
during swallowing [12]. Standardization of catheter
placement using the M wave has been documented in
numerous studies [2, 3, 5, 9]. Presence of the M wave
indicates placement of the third sensor at the proximal
border of the high-pressure zone of the cricopharyngeus
muscle [12]. UES measures made with the manometry
sensor in this position have been documented to most
closely reflect UES measures made using videofluoroscopy
[13]. Sensors were oriented toward the posterior pharyn-
geal wall [2, 3], as confirmed by continuous monitoring of
unidirectional markers on the catheter. The catheter was
then secured to the nose with medical tape. Sensor 1 was
therefore located in the upper pharynx (approximately even
with the base of the tongue), sensor 2 in the midpharynx
(approximately even with the laryngeal additus), and sen-
sor 3 in the proximal aspect of the tonically contracted UES
[14]. The distance from the third sensor to the nose tip for
session 1 was noted. For sessions 2 and 3, the catheter was
inserted into the same naris and to the same distance in
millimeters from the tip of the nose as was determined
optimal in session 1. Participants executed five dry swal-
lows and five 10-ml water bolus swallows in each session.
A 10-ml water bolus was chosen to provide a contrast in
volume to that of saliva swallows, which can be as much as
2 ml [15]. There is also evidence to suggest that bolus
volume may reach up to 10–12 ml during natural drinking
situations [16]. Participants were prompted to swallow
whenever they felt comfortable, following a 30-s rest
period. Participants were seated so they were unable to
view the waveforms displayed on the computer monitor.
P. R. Macrae et al.: Within-Subject Variance in Pharyngeal Pressures During Swallowing
123
Data Analysis
Peak or nadir pressures for each sensor were obtained
offline. These were defined as the highest (sensors 1 and 2)
or lowest (sensor 3) recorded pressure during each swal-
lowing event. Due to the open cavity formation of the
pharynx, contact pressure recordings were relative to
atmospheric pressure. As one of the two conditions eval-
uated in this study did not involve ingestion of a bolus and
as simultaneous fluoroscopy was not performed, pressure
measurements reflected contact pressure rather than intra-
bolus pressure. Contact pressure represents convergence of
the pharyngeal walls or the functional peristaltic wave of
the pharynx [17].
Statistical Analysis
Using the R statistical analysis environment [18], mixed-
effects models [19, 20] were used to estimate the order effects
and variability of the measures (both between sessions and
within a session). Confidence intervals were calculated for
both the order effects and the variability to indicate the degree
of uncertainty in the estimation of the parameters.
Results
Estimated baseline pressures (in mmHg with 95% confi-
dence intervals) for dry swallows were 95 (77–113), 114
Session and trial
Pre
ssur
e as
a fr
actio
n of
the
rang
e fo
r a
sens
or
0.0
0.2
0.4
0.6
0.8
1.0
0.0
0.2
0.4
0.6
0.8
1.0
0.0
0.2
0.4
0.6
0.8
1.0
0.0
0.2
0.4
0.6
0.8
1.0
0.0
0.2
0.4
0.6
0.8
1.0
0.01956
0.04376
0.04739
0.05566
0.07807
1 2 3
0.03756
0.04378
0.04893
0.05644
0.09262
1 2 3
0.03982
0.04394
0.04907
0.06040
0.09746
1 2 3
0.04182
0.04646
0.05041
0.06353
0.14154
1 2 3
variableSensor 1
Sensor 2
Sensor 3
Fig. 1 Individual values for
each of the five dry swallow
trials at each sensor for sessions
1, 2, and 3, for all 20
participants. Values have been
normalized to the range of
values at each sensor, to make
each value a percentage of the
range. Each plot is titled with
the individual mean of within-
session variance and progresses
from least variable to most
variable
P. R. Macrae et al.: Within-Subject Variance in Pharyngeal Pressures During Swallowing
123
(93–136), and -13 (-16 to -10) for sensors 1, 2, and 3,
respectively, and for 10-ml swallows they were 91
(70–112), 112 (90–133), and -8 (-11 to -5). Figure 1 dis-
plays individual values for all 20 participants for each of
the five trials plotted across each session for all three
sensors for dry swallows only, as dry swallows are repre-
sentative of both swallow types.
The variability within and across sessions is shown
in Table 1 as standard deviations with 95% confidence
intervals. Variability is greater across sessions than within
sessions for sensors 1 and 2 during both dry and 10-ml
swallows. The across-session variance measured at sensor
3 is relatively comparable to that measured within sessions.
There were no significant effects of trial or session at any
of the sensors for both dry and 10-ml swallows, with the
estimated maximum change no larger than 5% for trial and
no larger than 12% for session (Table 1).
To examine the relationship between within-session and
across-session variability, correlations of the two were
completed (Fig. 2). An individual’s maximum within-ses-
sion variance was plotted against the standard deviation for
the three sessions for that individual. The two were highly
correlated (r = 0.92, p \ 0.0001), with no difference
between the correlations for any of the three sensors.
Finally, an analysis was completed to probe the influ-
ence of identifying and deleting outliers from the data set.
From visual inspection of Fig. 1, sessions with a standard
deviation of approximately 20% or greater appeared to be
outliers in terms of session variance. Variance at this level
is proposed to reflect participant and/or catheter placement
issues based on the fact that stable measures could be
obtained for the same sensor in another session and/or a
different sensor in the same session. The complete data set
contains 20 participants, three sessions, three sensors, and
two conditions (dry and 10-ml swallows) totaling 360
participant-sensor-condition units. Ten of these units had a
within-session standard deviation greater than 20% and
were excluded to assess the effect of removing invalid
measures, leaving 350 participant-sensor-condition units.
Excluding these units reduced the confidence intervals
around value estimates; for example, at sensor 1 during
10-ml swallows, the initial 95% confidence interval for
the change over sessions of [-8.5 to 10.9] was reduced to
[-5.1 to 7.0], a decrease of 40%.
Discussion
This methodological study is the first to have determined
the within- and across-session variability of pharyngeal
contact pressure recordings during swallowing in normal
subjects. This information is important to the emergence of
manometry as a viable outcome measure in rehabilitation
research. The data presented here represent group vari-
ance for pharyngeal and UES pressures during normal
swallowing physiology and have relevance in interpreting
normative data of pharyngeal pressures provided by pre-
vious studies. Documenting this variance is important for
studies using healthy participants which investigate chan-
ges in pharyngeal function as a result of swallowing
maneuvers. These data are also important for formulating
power calculations for such studies, and for providing a
reference by which to compare dysphagic pharyngeal
pressure variation. These data suggest that peak and nadir
pressures change less than 2% due to order effects, with the
estimated maximal change not likely more than 5% in
consecutive trials and not more than 12% in consecutive
sessions. The data also suggest that for sensors 1 and 2,
variability is greater across sessions than within sessions.
Given the increased variability across sessions compared
with within a session, these data are important to consider
when using manometry for repeated measures to document
change as a result of treatments. The within-session vari-
ance documented here may also be useful for studies
wishing to compare the pressure generation associated
with different swallow techniques in the same session. As
Table 1 Within- and across-session variability in pharyngeal pressures along with estimated order effects for pharyngeal pressures
Swallow Sensor SD across trials
(mmHg)
Estimated change per
trial (mmHg)
SD across sessions
(mmHg)
Estimated change
per session (mmHg)
Dry 1 13.4 (12.2–14.8) 0.4 (-1.2 to 2.0) 18.5 (14.5–23.7) 1.0 (-5.2 to 7.2)
Dry 2 17.3 (15.8–18.9) -0.5 (-1.9 to 0.9) 27.5 (21.7–35.0) -1.0 (-10.1 to 8.2)
Dry 3 3.0 (2.8–3.3) -0.1 (-0.5 to 0.2) 3.6 (2.8–4.7) -0.3 (-1.5 to 1.0)
10-ml 1 16.3 (14.8–17.9) 1.6 (-0.5 to 3.6) 29.4 (23.2–37.2) 1.2 (-8.5 to 10.9)a
10-ml 2 17.7 (16.1–19.5) -1.6 (-3.3 to 0.1) 23.2 (18.1–29.8) -0.1 (-7.9 to 7.8)
10-ml 3 2.6 (2.4–2.9) -0.1 (-0.4 to 0.1)b 2.8 (2.2–3.7) -0.1 (-1.1 to 0.8)
Estimated values are shown with 95% confidence intervals in bracketsa Greatest change across sessions (12%)b Greatest change across trials (5%)
P. R. Macrae et al.: Within-Subject Variance in Pharyngeal Pressures During Swallowing
123
intrabolus pressure was not measured, the present findings
are applicable to contact pressure only.
One consideration in manometric evaluation of pha-
ryngeal pressures is the use of unidirectional versus
circumferential sensors. The present study used a 2.1-mm-
diameter round catheter housing unidirectional sensors.
Evidence of radial asymmetry of pharyngeal and UES
pressures suggests that circumferential pressure sensors may
be advantageous over unidirectional sensors [21, 22]. There
is further evidence suggesting an advantage of an ovoid
catheter in negating problems with radial asymmetry
[11, 12]; therefore, consideration of the manometry assem-
bly used in this study is warranted. Although circumferential
sensors alleviate the issue of radial pressure asymmetry, the
increased diameter required to accommodate the sensors
may counteract this advantage when looking at pressures in
the pharynx. Variation in manometric recordings has been
confirmed in relation to an increase in catheter diameter [23],
as well as in response to stress [24], which could arguably
play a role in the tolerance of a larger catheter. In addition,
bolus flow is influenced by catheter diameter [17], suggest-
ing that a smaller-diameter catheter may provide more rep-
resentative pharyngeal pressures related to swallowing.
Previous studies using the same catheter assembly as the
present study have shown consistent measures of pharyngeal
pressure [25]. Furthermore, the present study highlights that
by maintaining sensors in a posterior orientation, pressures
within the UES are relatively stable within and across ses-
sions, with no significant order effects and an estimated
maximum change of no more than 5% across trials and 12%
across sessions for all sensors. There is, however, reasonable
variance in pressures measured at all sensors. Comparing the
variance seen in the present study with that documented
using circumferential sensors would provide insight into
how different catheter placements are affected by radial
asymmetry in the pharynx.
The variance within and across sessions depicted in
Fig. 1 shows a larger variation of values for some sessions
than for others, and for some sensors more than others
within individuals. In order to provide empirical evidence
for dysphagia treatment techniques, outcome measures
need to be sensitive to changes in various swallowing
parameters. The considerable within- and across-session
variability documented in this study suggests that attempts
to validate treatments using pharyngeal manometry require
either substantial effect sizes and/or participant numbers. If
sources of variation can be identified and removed, the
application of results from studies incorporating pharyn-
geal manometry should be improved.
Causes of variation across session may relate to changes
in catheter placement. Doeltgen et al. [10] evaluated vari-
ation in catheter placement using radiographic still images.
In five of ten participants, repeat catheter placement did not
change catheter position in the pharynx. If their finding is
applied to the present study, with 50% of participants
showing varied catheter position in consecutive placements
in the pharynx, our data suggest this variance will likely
Maximum within-session variance
Bet
wee
n-se
ssio
n va
rianc
e
0.00
0.02
0.04
0.06
0.08
0.10
0.12
0.00
0.02
0.04
0.06
0.08
0.10
0.12
0.00
0.02
0.04
0.06
0.08
0.10
0.12
0.05 0.10 0.15 0.20 0.25
Sensor 1
Sensor 2
Sensor 3
swallow
10-ml swallow
Dry swallow
Fig. 2 Scatterplots of the relationship between within- and across-
session variability for sensors 1, 2, and 3. Within-session variability
reflects the largest individual within-session standard deviation.
Across-session variability is the standard deviation of the mean of
the three sessions
P. R. Macrae et al.: Within-Subject Variance in Pharyngeal Pressures During Swallowing
123
contribute to the increased variability seen in pressures
across sessions.
Variability within a participant could be influenced by
individual anatomy. Anatomical variations could predis-
pose measurements to the effects of catheter tolerance or
radial asymmetry. An interaction of differential catheter
placement and anatomical differences may create more
variation for one session and/or sensor compared with
others, as seen for the participant with mean within-session
variance of 0.055 in Fig. 1. Completing a similar investi-
gation using radiographs would further elucidate the
influence of catheter placement and anatomical differences
on the variation within and across sessions.
The highly predictive relationship between within- and
across-session variances suggests that utilizing individual
means of pharyngeal pressures for a given session/sensor
may not be the optimal first step in analysis of such data. If
the goal of the investigation is to reliably document change
in swallowing pressures as a result of intervention, then
assessing the within-session variability for individuals and
excluding high-variability sessions/sensors may result in
more definitive results. While excluding data is typically
not ideal in group analysis, and not generally possible in the
assessment of patients, it may be necessary for the purpose
of effective treatment evaluation. So as to avoid bias,
exclusion of data must be based on the inference that true
values of pharyngeal pressure are not being recorded. Fig-
ure 1 shows that while a given sensor may show substantial
variability for a given session, other sessions show very
reproducible values for the same sensor (see the participant
with mean within-session variance of 0.097, sensor 1,
Fig. 1). If high variability within sessions reflected true
variation inherent in each individual swallow, all sessions
should show similar variability for that sensor. The analysis
completed on a subset of these data showed that by elimi-
nating units (sensors for a given session and swallow type)
that varied more than 20% of the range for that sensor,
confidence intervals around values for that sensor were
substantially improved. By excluding these highly variable
units, it greatly increases the confidence that any change
over sessions is small. For treatment studies, large confi-
dence intervals increase the number of participants required
to accurately determine the effect of a treatment.
This study did not assess a range of bolus sizes, using
only a 10-ml water bolus. Sensor 3, where the lumen sur-
rounding the catheter is much smaller than in the pharynx,
is more likely to be influenced by the presence of a bolus.
However, within- and across-session variances were com-
parable across all sensors, for both dry and 10-ml water
swallows. Comparing the variations within and across
sessions documented in the present study with those of
future studies using circumferential sensors and various
bolus sizes would be of interest.
Provided that the variation reported in this study is
considered in analysis of group treatment effects, pharyn-
geal pressure recorded using manometry can provide a
valuable outcome measure for treatment studies. Because
this study did not assess pharyngeal pressures of patients
with dysphagia, the values here must be considered to
reflect normal swallowing physiology only. A meticulous
approach to validation of dysphagia management tech-
niques often involves initially documenting normal physi-
ology [26]. Therefore, although these findings are not
generalizable to the patient population per se, the data
represent a first step in investigating variability in mano-
metric measures of pharyngeal pressures. These data may
serve as a reference for the variability seen in patient
groups and a basis for analysis of further studies of healthy
participants. These data should also be considered in the
interpretation of normative data for pharyngeal pressures.
The large within- and across-subject variability docu-
mented here suggests that further studies in which this
variability is eliminated are needed to gain a clear under-
standing of treatment effects on pharyngeal pressures
before these treatments are applied to patients, where
variability may be greater.
Acknowledgments The research was conducted during the tenure
of a Postgraduate Scholarship of the New ZealandNeurological
Foundation, awarded to the first author, Phoebe Macrae.
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Phoebe R. Macrae BSLT(Hons)
Daniel J. Myall PhD
Richard D. Jones PhD
Maggie-Lee Huckabee PhD
P. R. Macrae et al.: Within-Subject Variance in Pharyngeal Pressures During Swallowing
123